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A plant virus manipulates the behavior of its whitefly vector to enhance its transmission efficiency and spread.

ABSTRACT: Plant viruses can produce direct and plant-mediated indirect effects on their insect vectors, modifying their life cycle, fitness and behavior. Viruses may benefit from such changes leading to enhanced transmission efficiency and spread. In our study, female adults of Bemisia tabaci were subjected to an acquisition access period of 72 h in Tomato yellow leaf curl virus (TYLCV)-infected and non-infected tomato plants to obtain viruliferous and non-viruliferous whiteflies, respectively. Insects that were exposed to virus-infected plants were checked by PCR to verify their viruliferous status. Results of the Ethovision video tracking bioassays indicated that TYLCV induced an arrestant behavior of B. tabaci, as viruliferous whitefly adults remained motionless for more time and moved slower than non-viruliferous whiteflies after their first contact with eggplant leaf discs. In fact, Electrical Penetration Graphs showed that TYLCV-viruliferous B. tabaci fed more often from phloem sieve elements and made a larger number of phloem contacts (increased number of E1, E2 and sustained E2 per insect, p<0.05) in eggplants than non-viruliferous whiteflies. Furthermore, the duration of the salivation phase in phloem sieve elements (E1) preceding sustained sap ingestion was longer in viruliferous than in non-viruliferous whiteflies (p<0.05). This particular probing behavior is known to significantly enhance the inoculation efficiency of TYLCV by B. tabaci. Our results show evidence that TYLCV directly manipulates the settling, probing and feeding behavior of its vector B. tabaci in a way that enhances virus transmission efficiency and spread. Furthermore, TYLCV-B. tabaci interactions are mutually beneficial to both the virus and its vector because B. tabaci feeds more efficiently after acquisition of TYLCV. This outcome has clear implications in the epidemiology and management of the TYLCV-B. tabaci complex.

SUBMITTER: Moreno-Delafuente A

PROVIDER: S-EPMC3629040 | biostudies-literature | 2013

REPOSITORIES: biostudies-literature

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A plant virus manipulates the behavior of its whitefly vector to enhance its transmission efficiency and spread.

Moreno-Delafuente Ana A Garzo Elisa E Moreno Aranzazu A Fereres Alberto A

PloS one 20130416 4

Plant viruses can produce direct and plant-mediated indirect effects on their insect vectors, modifying their life cycle, fitness and behavior. Viruses may benefit from such changes leading to enhanced transmission efficiency and spread. In our study, female adults of Bemisia tabaci were subjected to an acquisition access period of 72 h in Tomato yellow leaf curl virus (TYLCV)-infected and non-infected tomato plants to obtain viruliferous and non-viruliferous whiteflies, respectively. Insects th ...[more]

PMID: 23613872

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Project description:Apoptosis is generally considered the first line of defense against viral infection. However, the role of apoptosis in the interactions between plant viruses and their insect vectors has rarely been investigated. By studying plant DNA viruses of the genus Begomovirus within the family Geminiviridae, which are transmitted by whiteflies of the Bemisia tabaci species complex in a persistent manner, we revealed that virus-induced apoptosis in insect vectors can facilitate viral accumulation and transmission. We found that infection with tomato yellow leaf curl virus activated the apoptosis pathway in B. tabaci Suppressing apoptosis by inhibitors or silencing caspase-3 significantly reduced viral accumulation, while the activation of apoptosis increased viral accumulation in vivo Moreover, the positive effect of whitefly apoptosis on virus accumulation and transmission was not due to its cross talk with the autophagy pathway that suppresses begomovirus infection in whiteflies. We further showed that viral replication, rather than the viral coat protein, is likely the critical factor in the activation of apoptosis by the virus. These novel findings indicate that similarly to many animal and a few plant RNA viruses, plant DNA viruses may activate apoptosis in their insect vectors leading to enhanced viral accumulation and transmission.IMPORTANCE Of the approximately 1,100 known plant viruses, about one-third are DNA viruses that are vectored by insects. Plant virus infections often induce cellular and molecular responses in their insect vectors, which can, in many cases, affect the spread of viruses. However, the mechanisms underlying vector responses that affect virus accumulation and transmission are poorly understood. Here, we examined the role of virus-induced apoptosis in the transmission of begomoviruses, a group of single-stranded plant DNA viruses that are transmitted by whiteflies and cause extensive damage to many crops worldwide. We demonstrated that virus infection can induce apoptosis in the insect vector conferring protection to the virions from degradation, leading to enhanced viral accumulation and transmission to host plants. Our findings provide valuable clues for designing new strategies to block the transmission of insect-vectored plant viruses, particularly plant DNA viruses.

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A plant virus manipulates the behavior of its whitefly vector to enhance its transmission efficiency and spread.

Publications

A plant virus manipulates the behavior of its whitefly vector to enhance its transmission efficiency and spread.

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